Dissecting the Mechanisms of Cell Movements During Morphogenesis Public Deposited

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  • March 21, 2019
Creator
  • Roh, Minna
    • Affiliation: College of Arts and Sciences, Department of Biology
Abstract
  • How embryonic cells transition from spatial patterning to morphogenesis is a fascinating and incompletely understood topic. In C. elegans, the first morphogenetic movement is the internalization of two endodermal precursor cells (E cells). The current model for how these cells become internalized is that an apically-enriched population of activated non-muscle myosin II motors drives apical constriction, and this may pull a ring of six neighboring cells together to cover the free surfaces of the E cells. Depleting Arp2/3 complex in C. elegans results in gastrulation defects. Although Arp2/3 is known to function in morphogenesis in various developmental systems, its specific roles in motile cells during morphogenesis are not well understood. We have found that in Arp2/3 depleted C. elegans embryos, although the E cells do not fully internalize, the E cells have normal fate and apicobasal polarity. Non-muscle myosin II still accumulates and becomes activated in the apical region of the E cells. When analyzing actin dynamics, we found that half of the ring of six neighboring cells (three of the six cells) extends Arp2/3-dependent, short, dynamic, F-actin-rich structures near their apical borders with the E cells. These results suggest that in addition to apical constriction, E cell internalization may also involve migration of the neighboring cells. We also examined non-muscle myosin II dynamics to follow movements of myosin foci with respect to the zones where E cells contact their neighboring cells in wild-type embryos. We expected to observe narrowing of the contact zones in concert with contraction of the actomyosin network. We were surprised to find instead that centripetal myosin movements preceded narrowing of contact zones, contracting the apical actomyosin network multiple times over before significant neighboring cell movements. Later, myosin foci continued to coalesce centripetally and contact zones narrowed in concert. This suggests that a regulatable link (a clutch) may connect cortical actomyosin contraction to neighboring cell movements. To test this hypothesis, first, we tracked cell surface movements using fluorescent quantum dots. Our results suggest that free surfaces of E cells move together with cortical actomyosin contraction before neighboring cells move in concert, suggesting that the regulatable link lies between the E cell apical cytoskeleton and neighboring cells, and hence may be comprised of cell-cell adhesion complex proteins or proteins that link these complexes to the cytoskeleton. Second, we analyzed adhesion-defective embryos and found that coupling of myosin and contact zone dynamics fails. Together with the finding that similar centripetal myosin movements move polarity proteins toward the center of the apical surface at earlier embryonic stages, our results suggest that the transition from apicobasal cell polarization to cell internalization is governed by a molecular clutch.
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  • Goldstein, Robert P.
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